Skip to main content
Log in

Effect of glutamate transport and catabolism on symbiotic effectiveness in Rhizobium leguminosarum bv. phaseoli

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Seven Tn5 induced mutants unable to use glutamate as sole carbon and nitrogen source were isolated from the effective Rhizobium leguminosarum bv. phaseoli strain P121-R. As indicated by restriction and hybridisation analysis, all the mutants arose from a single Tn5 insertion in the chromosome. The 14C-glutamate uptake rate of the mutants was 76 to 88% lower than that of strain P121-R. Inoculation of Phaseolus vulgaris cv. Labrador with these mutants significantly decreased shoot dry matter yield and the total nitrogen content respectively, as compared to inoculation with the parental strain P121-R. All the mutants formed nodules, however they were smaller, white to greenish and approximately 30% less numerous than those formed by strain P121-R. These observations suggest that glutamate transport and catabolism in R. leguminosarum bv. phaseoli P121-R may play an important role in the establishment of an effective symbiosis in field bean. None of the mutants isolated was an auxotroph. All mutants were unable to grow on aspartate suggesting that glutamate and aspartate, probably have the same transporter as indicated in Rhizobium meliloti and in Bacillus subtilis. All mutants readily used glutamine, proline, arginine as sole carbon and nitrogen source, but grew more slowly than the wild type strain. On the other hand, all the mutants were impaired in growth on histidine and γ-aminobutyrate as sole carbon and nitrogen source. As the catabolism of these amino acids occurs predominantly through glutamate, our results indicate that mutants are also impaired in their ability to use histidine and γ-aminobutyrate as a nitrogen source. Our results also suggest that other amino acids catabolized through the glutamate pathways may be an additional important carbon source for bacteroids in nodules.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Antoun H, Bordeleau L M and Sauvageau R 1984 Utilization of the tricarboxylic acid cycle intermediates and symbiotic effectiveness in Rhizobium meliloti. Plant and Soil 77, 29–38.

    Google Scholar 

  • Bergersen F J and Turner G L 1988 Glutamate as a carbon source for N2-fixing bacteroids prepared from soybean nodules. J. Gen. Microbiol. 134, 2441–2448.

    Google Scholar 

  • Beringer J E 1974 R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84, 188–198.

    Google Scholar 

  • Bigwaneza P C, Prévost D, Bordeleau L M and Antoun H 1991 Glucose transport by an arctic and a temperate strain of rhizobia. Can. J. Microbiol. 37, 105–109.

    Google Scholar 

  • Bigwaneza P C, Prévost D, Bordeleau L M and Antoun H 1993 Effect of temperature on succinate transport by an arctic and a temperature strain of rhizobia. Can. J. Microbiol. 39, 907–911.

    Google Scholar 

  • Bordeleau L M, Antoun H and Lachance R A 1977 Effets des souches de Rhizobium meliloti et des coupes successives de la luzerne (Medicago sativa) sur la fixation symbiotique d'azote. Can. J. Plant Sci. 57, 433–439.

    Google Scholar 

  • Chao W L, Nelson E B, Harnzan G E and Hoch H C 1986 Colonization of the rhizosphere by biological control agents applied to seeds. Phytopathology 76, 60–65.

    Google Scholar 

  • Dilworth M J, Arwas R, McKay I A, Saroso S and Glenn A R 1986 Pentose metabolism in Rhizobium leguminosarum MNF3OO and in cowpea Rhizobium NGR234. J. Gen. Microbiol. 132, 2733–2742.

    Google Scholar 

  • Fitzmaurice A M and O'Gara F 1991 Glutamate catabolism in Rhizobium meliloti. Arch. Microbiol. 155, 422–427.

    Google Scholar 

  • Fitzmaurice A M and O'Gara F 1993 A Rhizobium meliloti mutant lacking a functional γ-aminobutyrate (GABA) bypass, is defective in glutamate catabolism and symbiotic nitrogen fixation. FEMS Microbiol. Lett. 109, 195–202.

    Google Scholar 

  • Kahn M L, Kraus J and Sommerville J E 1985 A model of nutrient exchange in the Rhizobium-legume symbiosis. In Nitrogen Fixation Research Progress. Eds. H JEvans, P JBottomley and W ENewton. pp 193–199. Martinus Nijhoff, Dordrecht, the Netherlands.

    Google Scholar 

  • Laberge S, Gagnon Y, Bordeleau L M and Lapointe J 1989 Cloning and sequencing of the gltX gene, encoding the glutamyl-tRNA synthetase of Rhizobium meliloti A2. J. Bacteriol. 171, 3926–3932.

    Google Scholar 

  • Lafontaine P J, Lafrenière C and Antoun H 1989 Some properties of carbohydrate and C4-dicarboxylic acid utilization negative mutants of Rhizobium leguminosarum biovar phaseoli strain P 121. Plant and Soil 120, 195–201.

    Google Scholar 

  • Lafrenière C, Lafontaine P, Marion C and Antoun H 1987 Oxidation of substrates in organic acids utilization negative mutants and the wild type Rhizobium meliloti strain S14. Plant and Soil 101, 73–78.

    Google Scholar 

  • Lalande R, Antoun H, Paré T and Joyal P 1988 Effets de l'inoculation avec des souches du Rhizobium leguminosarum biovar phaseoli sur le rendement et la teneur en azote du haricot (Phaseolus vulgaris). Nat. Can. (Rev. Écol. Syst.) 113, 337–346.

    Google Scholar 

  • Maniatis R, Fritsch E F and Sambrook J 1982 Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

    Google Scholar 

  • Poole P S, Franklin M, Glenn A R and Dilworth M J 1985 The transport of L-glutamate by Rhizobium leguminosarum involves a common amino acid carrier. J. Gen. Microbiol. 131, 1441–1448.

    Google Scholar 

  • Rastogi V K and Watson R J 1991 Aspartate aminotransferase activity is required for aspartate catabolism and symbiotic nitrogen fixation in Rhizobium meliloti. J. Bacteriol. 173, 2879–2887.

    Google Scholar 

  • Salminen S O and Streeter J G 1987 Involvement of glutamate in the respiratory metabolism of Bradyrhizobium japonicum bacteroids. J. Bacteriol. 169, 495–499.

    Google Scholar 

  • Salminen S O and Streeter J G 1990 Factors contributing to the accumulation of glutamate in Bradyrizobium japonicum bacteroids under microaerobic conditions. J. Gen. Microbiol. 136, 2119–2126.

    Google Scholar 

  • Simon R, Priefer U and Pühler A 1983 Vector plasmids for in-vivo and in-vitro manipulations of gram-negative bacteria. In Molecular-Genetics of the Bacteria-Plant Interaction. Ed. APühler. pp 98–106. Springer, Verlag, Germany.

    Google Scholar 

  • Streeter J G 1991 Transport and metabolism of carbon and nitrogen in legume nodules. Adv. Bot. Res. 18, 129–187.

    Google Scholar 

  • Tolner B, Ubbink-Kok T, Poolman B and Konings W N 1995 Characterization of the proton/glutamate symport protein of Bacillus subtilis and its functional expression in Escherichia coli. J. Bacteriol. 177 2863–2869.

    Google Scholar 

  • Vance C P and Heichel G H 1991 Carbon in N2 fixation: limitation or exquisite adaptation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 373–392.

    Google Scholar 

  • Watson R J, Rastogi V K and Chan Y-K 1993. Aspartate transport in Rhizobium meliloti. J. Gen. Microbiol. 139, 1315–1323.

    Google Scholar 

  • Werner D 1992 Physiology of nitrogen-fixing legume nodules: compartments and functions. In Biological Nitrogen Fixation. Eds. GStacey, R HBurris and H JEvans. pp 399–431. Chapman and Hall, New York.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Labidi, M., Lalande, R., Laberge, S. et al. Effect of glutamate transport and catabolism on symbiotic effectiveness in Rhizobium leguminosarum bv. phaseoli . Plant Soil 182, 51–58 (1996). https://doi.org/10.1007/BF00010994

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00010994

Key words

Navigation